Literature DB >> 17179040

Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements.

Evan A Zamir1, András Czirók, Cheng Cui, Charles D Little, Brenda J Rongish.   

Abstract

Gastrulation is a fundamental process in early development that results in the formation of three primary germ layers. During avian gastrulation, presumptive mesodermal cells in the dorsal epiblast ingress through a furrow called the primitive streak (PS), and subsequently move away from the PS and form adult tissues. The biophysical mechanisms driving mesodermal cell movements during gastrulation in amniotes, notably warm-blooded embryos, are not understood. Until now, a major challenge has been distinguishing local individual cell-autonomous (active) displacements from convective displacements caused by large-scale (bulk) morphogenetic tissue movements. To address this problem, we used multiscale, time-lapse microscopy and a particle image velocimetry method for computing tissue displacement fields. Immunolabeled fibronectin was used as an in situ marker for quantifying tissue displacements. By imaging fluorescently labeled mesodermal cells and surrounding extracellular matrix simultaneously, we were able to separate directly the active and passive components of cell displacement during gastrulation. Our results reveal the following: (i) Convective tissue motion contributes significantly to total cell displacement and must be subtracted to measure true cell-autonomous displacement; (ii) Cell-autonomous displacement decreases gradually after regression from the PS; and (iii) There is an increasing cranial-to-caudal (head-to-tail) cell-autonomous motility gradient, with caudal cells actively moving away from the PS faster than cranial cells. These studies show that, in some regions of the embryo, total mesodermal cell displacements are mostly due to convective tissue movements; thus, the data have profound implications for understanding cell guidance mechanisms and tissue morphogenesis in warm-blooded embryos.

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Year:  2006        PMID: 17179040      PMCID: PMC1705812          DOI: 10.1073/pnas.0606100103

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  18 in total

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Journal:  Methods Mol Biol       Date:  2000

Review 2.  The vertebrate segmentation clock.

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3.  Quantitative evaluation of convolution-based methods for medical image interpolation.

Authors:  E H Meijering; W J Niessen; M A Viergever
Journal:  Med Image Anal       Date:  2001-06       Impact factor: 8.545

4.  Culturing of avian embryos for time-lapse imaging.

Authors:  Paul A Rupp; Brenda J Rongish; Andras Czirok; Charles D Little
Journal:  Biotechniques       Date:  2003-02       Impact factor: 1.993

5.  Multi-field 3D scanning light microscopy of early embryogenesis.

Authors:  A Czirók; P A Rupp; B J Rongish; C D Little
Journal:  J Microsc       Date:  2002-06       Impact factor: 1.758

Review 6.  Quantitative motion analysis and visualization of cellular structures.

Authors:  Daniel Gerlich; Julian Mattes; Roland Eils
Journal:  Methods       Date:  2003-01       Impact factor: 3.608

7.  Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation.

Authors:  Diane S Sepich; Colette Calmelet; Maria Kiskowski; Lila Solnica-Krezel
Journal:  Dev Dyn       Date:  2005-10       Impact factor: 3.780

8.  A digital image-based method for computational tissue fate mapping during early avian morphogenesis.

Authors:  Evan A Zamir; András Czirók; Brenda J Rongish; Charles D Little
Journal:  Ann Biomed Eng       Date:  2005-06       Impact factor: 3.934

9.  A series of normal stages in the development of the chick embryo.

Authors:  V HAMBURGER; H L HAMILTON
Journal:  J Morphol       Date:  1951-01       Impact factor: 1.804

10.  Assembly and remodeling of the fibrillar fibronectin extracellular matrix during gastrulation and neurulation in Xenopus laevis.

Authors:  Lance A Davidson; Raymond Keller; Douglas W DeSimone
Journal:  Dev Dyn       Date:  2004-12       Impact factor: 3.780

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  58 in total

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Journal:  J Cell Sci       Date:  2011-12-01       Impact factor: 5.285

2.  Not just inductive: a crucial mechanical role for the endoderm during heart tube assembly.

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Journal:  Development       Date:  2012-05       Impact factor: 6.868

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Authors:  Anastasia Sacharidou; Amber N Stratman; George E Davis
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4.  Mechanics of head fold formation: investigating tissue-level forces during early development.

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Journal:  Dev Biol       Date:  2012-01-04       Impact factor: 3.582

6.  Invasion from a cell aggregate--the roles of active cell motion and mechanical equilibrium.

Authors:  A Szabó; K Varga; T Garay; B Hegedus; A Czirók
Journal:  Phys Biol       Date:  2012-02-07       Impact factor: 2.583

7.  Extracellular matrix fluctuations during early embryogenesis.

Authors:  A Szabó; P A Rupp; B J Rongish; C D Little; A Czirók
Journal:  Phys Biol       Date:  2011-07-12       Impact factor: 2.583

8.  Vascular sprout formation entails tissue deformations and VE-cadherin-dependent cell-autonomous motility.

Authors:  Erica D Perryn; András Czirók; Charles D Little
Journal:  Dev Biol       Date:  2007-11-04       Impact factor: 3.582

Review 9.  Multicellular sprouting during vasculogenesis.

Authors:  Andras Czirok; Evan A Zamir; Andras Szabo; Charles D Little
Journal:  Curr Top Dev Biol       Date:  2008       Impact factor: 4.897

10.  Fast fluorescence microscopy for imaging the dynamics of embryonic development.

Authors:  Julien Vermot; Scott E Fraser; Michael Liebling
Journal:  HFSP J       Date:  2008-05-13
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